Perturbed MafB/GATA1 axis after burn trauma bares the potential mechanism for immune suppression and anemia of critical illness

Journal of Leukocyte Biology

Volumn 100, Issue 4, 2016, Pages 725-736

  Johnson, Nicholas B ^a   Posluszny, Joseph A ^b,c   He, Li K ^b,c   Szilagyi, Andrea ^c   Gamelli, Richard L ^b,c   Shankar, Ravi ^b,c   Muthumalaiappan, Kuzhali ^b,c  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

^c MOUNT SINAI HOSPITAL   (United States)

Author keywords

CMP; Dendritic cell; Hematopoiesis; Macrophages; MEP

Indexed keywords

SMALL INTERFERING RNA; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR MAFB; COLONY STIMULATING FACTOR RECEPTOR; GATA1 PROTEIN, MOUSE; HYBRID PROTEIN; MAFB PROTEIN, MOUSE;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BURN; BURN PATIENT; CELL DIFFERENTIATION; CONTROLLED STUDY; CRITICAL ILLNESS; ERYTHROPOIESIS; GENE SILENCING; GRANULOCYTE; HEMATOCRIT; HEMATOPOIESIS; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MACROPHAGE; MALE; MEGAKARYOCYTE; MONOCYTE; MONOCYTOSIS; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEADY STATE; ANIMAL; BIOSYNTHESIS; BLOOD; CELL CULTURE; CELL LINEAGE; DENDRITIC CELL; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; METABOLISM; MYELOPOIESIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RNA INTERFERENCE;

ANEMIA; ANIMALS; BURNS; CELL LINEAGE; CELLS, CULTURED; CRITICAL ILLNESS; DENDRITIC CELLS; GATA1 TRANSCRIPTION FACTOR; MACROPHAGES; MAFB TRANSCRIPTION FACTOR; MALE; MICE; MONOCYTES; MYELOID PROGENITOR CELLS; MYELOPOIESIS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC;

EID: 84990065073     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1A0815-377R     Document Type: Article

References (44)

1. Oberholzer, A., Oberholzer, C., Moldawer, L. L. (2001) Sepsis syndromes: understanding the role of innate and acquired immunity. Shock 16, 83-96.
2. Munoz, C., Carlet, J., Fitting, C., Misset, B., Blériot, J. P., Cavaillon, J. M. (1991) Dysregulation of in vitro cytokine production by monocytes during sepsis. J. Clin. Invest. 88, 1747-1754.
3. Baue, A. E., Durham, R., Faist, E. (1998) Systemic inflammatory response syndrome (SIRS), multiple organ dysfunction syndrome (MODS), multiple organ failure (MOF): are we winning the battle? Shock 10, 79-89.
4. Astin, R., Puthucheary, Z. (2014) Anaemia secondary to critical illness: an unexplained phenomenon. Extrem. Physiol. Med. 3, 4.
5. Corwin, H. L., Gettinger, A., Pearl, R. G., Fink, M. P., Levy, M. M., Abraham, E., MacIntyre, N. R., Shabot, M. M., Duh, M. S., Shapiro, M. J. (2004) The CRIT Study: anemia and blood transfusion in the critically ill-current clinical practice in the United States. Crit. Care Med. 32, 39-52.
6. Kwan, P., Gomez, M., Cartotto, R. (2006) Safe and successful restriction of transfusion in burn patients. J. Burn Care Res. 27, 826-834.
7. Curinga, G., Jain, A., Feldman, M., Prosciak, M., Phillips, B., Milner, S. (2011) Red blood cell transfusion following burn. Burns 37, 742-752.
8. American Burn Association Burn Multicenter Trials Group. (2006) Effect of blood transfusion on outcome after major burn injury: a multicenter study. Crit. Care Med. 34, 1602-1607.
9. ABC (Anemia and Blood Transfusion in Critical Care) Investigators. (2002) Anemia and blood transfusion in critically ill patients. JAMA 288, 1499-1507.
10. Kupper, T. S., Green, D. R., Durum, S. K., Baker, C. C. (1985) Defective antigen presentation to a cloned T helper cell by macrophages from burned mice can be restored with interleukin-1. Surgery 98, 199-206.
11. Sachse, C., Prigge, M., Cramer, G., Pallua, N., Henkel, E. (1999) Association between reduced human leukocyte antigen (HLA)-DR expression on blood monocytes and increased plasma level of interleukin-10 in patients with severe burns. Clin. Chem. Lab. Med. 37, 193-198.
12. Zapata-Sirvent, R. L., Hansbrough, J. F. (1993) Temporal analysis of human leucocyte surface antigen expression and neutrophil respiratory burst activity after thermal injury. Burns 19, 5-11.
13. De, A. K., Laudanski, K., Miller-Graziano, C. L. (2003) Failure of monocytes of trauma patients to convert to immature dendritic cells is related to preferential macrophage-colony-stimulating factor-driven macrophage differentiation. J. Immunol. 170, 6355-6362.
14. Poehlmann, H., Schefold, J. C., Zuckermann-Becker, H., Volk, H. D., Meisel, C. (2009) Phenotype changes and impaired function of dendritic cell subsets in patients with sepsis: a prospective observational analysis. Crit. Care 13, R119.
15. D’Arpa, N., Accardo-Palumbo, A., Amato, G., D’Amelio, L., Pileri, D., Cataldo, V., Mogavero, R., Lombardo, C., Napoli, B., Conte, F. (2009) Circulating dendritic cells following burn. Burns 35, 513-518.
16. Muthu, K., He, L. K., Melstrom, K., Szilagyi, A., Gamelli, R. L., Shankar, R. (2008) Perturbed bone marrow monocyte development following burn injury and sepsis promote hyporesponsive monocytes. J. Burn Care Res. 29, 12-21.
17. Hotchkiss, R. S., Tinsley, K. W., Swanson, P. E., Grayson, M. H., Osborne, D. F., Wagner, T. H., Cobb, J. P., Coopersmith, C., Karl, I. E. (2002) Depletion of dendritic cells, but not macrophages, in patients with sepsis. J. Immunol. 168, 2493-2500.
18. Howell, K., Posluszny, J., He, L. K., Szilagyi, A., Halerz, J., Gamelli, R. L., Shankar, R., Muthu, K. (2012) High MafB expression following burn augments monocyte commitment and inhibits DC differentiation in hemopoietic progenitors. J. Leukoc. Biol. 91, 69-81.
19. Williams, K. N., Szilagyi, A., He, L. K., Conrad, P., Halerz, M., Gamelli, R. L., Shankar, R., Muthumalaiappan, K. (2012) Dendritic cell depletion in burn patients is regulated by MafB expression. J. Burn Care Res. 33, 747-758.
20. Gamelli, R. L., Hebert, J. C., Foster, R. S., Jr. (1985) Effect of burn injury on granulocyte and macrophage production. J. Trauma 25, 615-619.
21. Peterson, V., Hansbrough, J., Buerk, C., Rundus, C., Wallner, S., Smith, H., Robinson, W. A. (1983) Regulation of granulopoiesis following severe thermal injury. J. Trauma 23, 19-24.
22. Santangelo, S., Gamelli, R. L., Shankar, R. (2001) Myeloid commitment shifts toward monocytopoiesis after thermal injury and sepsis. Ann. Surg. 233, 97-106.
23. Shoup, M., Weisenberger, J. M., Wang, J. L., Pyle, J. M., Gamelli, R. L., Shankar, R. (1998) Mechanisms of neutropenia involving myeloid maturation arrest in burn sepsis. Ann. Surg. 228, 112-122.
24. Wu, J. C., Livingston, D. H., Hauser, C. J., Deitch, E. A., Rameshwar, P. (2001) Trauma inhibits erythroid burst-forming unit and granulocytemonocyte colony-forming unit growth through the production of TGFbeta1 by bone marrow stroma. Ann. Surg. 234, 224-232.
25. Toliver-Kinsky, T. E., Cui, W., Murphey, E. D., Lin, C., Sherwood, E. R. (2005) Enhancement of dendritic cell production by fms-like tyrosine kinase-3 ligand increases the resistance of mice to a burn wound infection. J. Immunol. 174, 404-410.
26. Onai, N., Obata-Onai, A., Schmid, M. A., Ohteki, T., Jarrossay, D., Manz, M. G. (2007) Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8, 1207-1216.
27. Fogg, D. K., Sibon, C., Miled, C., Jung, S., Aucouturier, P., Littman, D. R., Cumano, A., Geissmann, F. (2006) A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311, 83-87.
28. Akashi, K., Traver, D., Miyamoto, T., Weissman, I. L. (2000) A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404, 193-197.
29. Onai, N., Manz, M. G., Schmid, M. A. (2010) Isolation of common dendritic cell progenitors (CDP) from mouse bone marrow. Methods Mol. Biol. 595, 195-203.
30. Muthu, K., He, L. K., Szilagyi, A., Stevenson, J., Gamelli, R. L., Shankar, R. (2009) Propranolol restores the tumor necrosis factor-alpha response of circulating inflammatory monocytes and granulocytes after burn injury and sepsis. J. Burn Care Res. 30, 8-18.
31. Posluszny, J. A., Jr., Muthumalaiappan, K., Kini, A. R., Szilagyi, A., He, L. K., Li, Y., Gamelli, R. L., Shankar, R. (2011) Burn injury dampens erythroid cell production through reprioritizing bone marrow hematopoietic response. J. Trauma 71, 1288-1296.
32. Raabe, B. M., Artwohl, J. E., Purcell, J. E., Lovaglio, J., Fortman, J. D. (2011) Effects of weekly blood collection in C57BL/6 mice. J. Am. Assoc. Lab. Anim. Sci. 50, 680-685.
33. D’Amico, A., Wu, L. (2003) The early progenitors of mouse dendritic cells and plasmacytoid predendritic cells are within the bone marrow hemopoietic precursors expressing Flt3. J. Exp. Med. 198, 293-303.
34. Posluszny, J. A., Jr., Gamelli, R. L. (2010) Anemia of thermal injury: combined acute blood loss anemia and anemia of critical illness. J. Burn Care Res. 31, 229-242.
35. Williams, K. N., Szilagyi, A., Conrad, P., Halerz, M., Kini, A. R., Li, Y., Gamelli, R. L., Shankar, R., Muthumalaiappan, K. (2013) Peripheral blood mononuclear cell-derived erythroid progenitors and erythroblasts are decreased in burn patients. J. Burn Care Res. 34, 133-141.
36. Bateman, A. P., McArdle, F., Walsh, T. S. (2009) Time course of anemia during six months follow up following intensive care discharge and factors associated with impaired recovery of erythropoiesis. Crit. Care Med. 37, 1906-1912.
37. Geissmann, F., Manz, M. G., Jung, S., Sieweke, M. H., Merad, M., Ley, K. (2010) Development of monocytes, macrophages, and dendritic cells. Science 327, 656-661.
38. Naik, S. H., Sathe, P., Park, H. Y., Metcalf, D., Proietto, A. I., Dakic, A., Carotta, S., O’Keeffe, M., Bahlo, M., Papenfuss, A., Kwak, J. Y., Wu, L., Shortman, K. (2007) Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8, 1217-1226.
39. Olweus, J., BitMansour, A., Warnke, R., Thompson, P. A., Carballido, J., Picker, L. J., Lund-Johansen, F. (1997) Dendritic cell ontogeny: a human dendritic cell lineage of myeloid origin. Proc. Natl. Acad. Sci. USA 94, 12551-12556.
40. Shen, H., de Almeida, P. E., Kang, K. H., Yao, P., Chan, C. W. (2012) Burn injury triggered dysfunction in dendritic cell response to TLR9 activation and resulted in skewed T cell functions. PLoS One 7, e50238.
41. Wilson, N. S., El-Sukkari, D., Villadangos, J. A. (2004) Dendritic cells constitutively present self antigens in their immature state in vivo and regulate antigen presentation by controlling the rates of MHC class II synthesis and endocytosis. Blood 103, 2187-2195.
42. Blanchi, B., Kelly, L. M., Viemari, J. C., Lafon, I., Burnet, H., Bévengut, M., Tillmanns, S., Daniel, L., Graf, T., Hilaire, G., Sieweke, M. H. (2003) MafB deficiency causes defective respiratory rhythmogenesis and fatal central apnea at birth. Nat. Neurosci. 6, 1091-1100.
43. Sieweke, M. H., Tekotte, H., Frampton, J., Graf, T. (1996) MafB is an interaction partner and repressor of Ets-1 that inhibits erythroid differentiation. Cell 85, 49-60.
44. Zhang, P., Zhang, X., Iwama, A., Yu, C., Smith, K. A., Mueller, B. U., Narravula, S., Torbett, B. E., Orkin, S. H., Tenen, D. G. (2000) PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood 96, 2641-2648.